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Advances in Oceanography and Limnology Vol. 3, No. 1, June 2012, 1–15
Strategies and mechanisms of resistance to viruses in photosynthetic aquatic microorganisms Rozenn Thomasab, Ste´phan Jacquetc, Nigel Grimsleyab and Herve´ Moreauab* a
CNRS, UMR 7232, Biologie inte´grative des organismes marins, Observatoire Oce´anologique, Avenue du Fontaule´, 66650 Banyuls-sur-Mer, France; bUPMC Univ Paris 06, UMR 7332, Biologie inte´grative des organismes marins, Observatoire Oce´anologique, Avenue du Fontaule´, 66650 Banyuls-sur-Mer, France; cINRA, UMR 42 CARRTEL, 75 avenue de Corzent, 74200 Thonon-les-Bains, France (Received 30 January 2012; final version received 29 February 2012) Surviving viral attack is essential for any species to avoid its irreversible removal from the ecosystem, and microbes must involve the resistance or susceptibility of individual cells. The co-existence between viruses and their hosts has led to the evolution of complex viral attack and host defence strategies. We review the state of the art about our understanding of resistance to viruses in aquatic eukaryotic photosynthetic microorganisms for which no synthesis has been provided yet, with comparisons to what is known for (cyano)bacteria or archaea. We discuss the cost of viral resistance to host cells, pointing out why it is important to consider its effect in studies of aquatic ecosystems, and how this may lead to a better understanding of population growth, structure, succession and blooms. The evolutionary consequences of resistance in the host-virus interactions are then reviewed, before considering possible perspectives for future research. Keywords: resistance; plankton; viruses; aquatic ecosystems
Introduction Phytoplankton is responsible for about half of the photosynthetic activity on Earth [1,2], the second half being assured by terrestrial plants. The striking difference between these two compartments is that marine (aquatic in a broader sense) photosynthesis, in contrast to its terrestrial counterpart, is mainly assumed by unicellular organisms, including both prokaryotes (e.g. cyanobacteria) and eukaryotes [3,4]. Viruses infect a large variety of aquatic prokaryotic and eukaryotic primary producers such as cyanobacteria, diatoms, cryptophytes, prasinophytes and prymnesiophytes [5–7] and evidence that viruses play critical roles in aquatic ecosystems has accumulated over the last two decades [8, and references therein]. Estimates for total lysis rate in phytoplankton populations vary widely in time and space [6–8], but viruses do play an important role in algal bloom control, regulation and termination [9–11]. As an example, in Emiliania huxleyi blooms, up to 50% of the cells were visibly infected by viruses during the decaying phase of the bloom [9,12] and blooms of this species are terminated by viruses [9,11,13]. Viruses infecting phytoplankton are extremely diverse [14], and most of the viruses infecting eukaryotic
*Corresponding author. Email:
[email protected] ISSN 1947–5721 print/ISSN 1947–573X online ß 2012 Taylor & Francis http://dx.doi.org/10.1080/19475721.2012.672338 http://www.tandfonline.com
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phytoplankton are reported to be members of the Phycodnaviridae family (‘‘phyco’’ from their algal hosts, ‘‘dna’’ because they have DNA genomes) [15–17]. However, several examples of RNA viruses infecting eukaryotic microalgae are also known [reviewed in 18], such as in diatoms [19,20], in the harmful red-tide dinoflagellates Heterocapsa circularisquama [21] and Heterocapsa akashiwo [22] and in the chlorophyte Micromonas [6]. Viruses infecting microorganisms display three main kinds of lifecycles: lytic, lysogenic and chronic [7]. The lytic cycle is, by far, better known for eukaryotic phytoplankton, probably not because it is more frequent but because it is the easiest to study. Indeed, during the lytic cycle, viruses proliferate until the lysis of the host cell and their release, thus it is easy to visualize and count this mortality, for example by plaque-forming units [23,24] where phytoplanktonic cells grow on agar plates and lysis appears as cleared circular regions (plaques) on the plate. Viral-induced mortality can also be counted by electron transmission microscopy [25] or throughout the modified dilution method [26,27] using flow cytometry. On the other hand, so far, the lysogenic cycle has been well described only in heterotrophic prokaryotic hosts [7] in contrast to autotrophs [28] even if the integration of a virus genome (circular dsDNA virus of 320 kb) into host genome has been reported for the macroalgae Ectocarpus siliculosus [29]. A similar situation to lysogeny results from a carrier state or pseudolysogeny [7], where a virus is latent in the host cell but is not integrated into the host genome. This state has been mentioned for Paramecium bursaria Chlorella Virus PBCV-1 [30,31]. Chronic infection involving viruses which are episodically or constantly released from the host cell, but without lysing it, is common in metazoan viruses. Such infection strategy has been extensively studied in medical virology, for example, in the Herpes and Hepatitis viruses [32]. In the aquatic environment, Mackinder et al. [33] found that Emiliania huxleyi virus (EhV) is released via budding, so that EhV particles are coated in lipid membrane, but this chronic cycle ends as a lysis of the host cell. Recently, chronic infection without host lysis has been reported by some of us for the first time in a marine primary producer Ostreococcus tauri, where cells release viruses through budding and without lysis of the host [34], allowing a stable coexistence between host and its virus. Strategies of resistance Molecular details of prokaryotic resistance to viruses have been elucidated in certain terrestrial host-pathogen systems [see 35 for an overview] but here we focus on aquatic ecosystems. Many excellent reviews on aquatic viruses have been written during the last 10–15 years [see 8 for references], mainly about the important roles of viruses (both phages and eukaryotic viruses) but, to our knowledge, the specific aspect of cell resistance to viral attack has only been briefly discussed in single publications [7,36,37]. Here we review mechanisms of resistance of both prokaryotic (cyanobacteria) and eukaryotic phytoplankton and consider each step in the viral cycle, including adsorption to the host cell surface, viral DNA entry, and viral replication or release, as any of these steps might form a barrier to viral propagation. Waterbury and Valois [38] first observed that populations of Synechococcus inoculated with different cyanophage populations were not affected by these viruses, and suggested that a preponderance of resistant cells might account for this. Further studies [39,40] subsequently confirmed that despite abundant cyanophage populations, relatively few bacterial cells were lysed (
